Eur. J. Entomol. 96: 57—68, 1999 ISSN 1210-5759

Larvae ofAtaenius (Coleóptera: : ): Generic characteristics and species descriptions

José R. VERDÚ and E duardo GALANTE

Departamento de Ciencias Ambientales y Recursos Naturales, Universidad de Alicante, E-03080 Alicante, Spain

Key words.Scarabaeidae, Aphodiinae, Ataenius, larvae, description, key, dung , turfgrass beetles,

Abstract. We compared the larval morphology of the genera Ataenius and Aphodius. The third larval instars of five Ataenius species: Ataenius opatrinus Harold, A. picinus Harold, A. platensis (Blanchard), A. simulator Harold and A. strigicauda Bates, are described or redescribed and illustrated. The most important morphological characteristics of the larvae of Ataenius are found in the respiratory plate of thoracic spiracle, the setation of venter of the last abdominal segment, the setation of the epicranial region and the morphology of the epipharynx. A key to larvae of the known species of Ataenius is included.

INTRODUCTION del Sacramento (Uruguay). For the purpose of laboratory studies, a total of 10 to 20 adult specimens of each species were The Ataenius Harold comprises 320 species, of kept in cylindrical plastic breeding cages (20 cm high, 10 cm which 228 species are found in America, 49 in Australia, wide) with moist soil and dry cow dung from which they had 11 in Africa, 6 in East Asia, 2 in Madagascar, and single been collected. The lid was an opening (6 cm diameter) covered species in India, Sri Lanka, Turkestan, Japan, Hawaii and with gauze screen. These breeding cages were maintained in an Sumatra, respectively (Dellacasa, 1987). Despite the rich­ environmental chamber at 25 : 20°C (L : D), 80 ± 5% RH, with ness of this genus and its worldwide distribution, the lar­ a photoperiod of 15 : 9 (L : D). The breeding cages were exam­ val morphology of only 7 species is known at present ined weekly and the results recorded. Throughout the study pe­ (Jerath, 1960; Ritcher, 1966). The life historieso f Ataen­ riod, complementary data were obtained in the field. Voucher specimens are deposited in the Collection of Entomology of the ius species are not well known, but some records indicate Departamento de Ciencias Ambientales y Recursos Naturales, that they are humus- and root-feeders in soil, with a few Universidad de Alicante, Spain (C.E.U.A.). species attracted to decaying vegetation and dung (Wegner & Niemczyk, 1981; Ratcliffe, 1991). Some spe­ Laboratory studies cies have been captured in ant nests and animal burrows Larval specimens were fixed in KAAD solution (Carne, 1951) (Cartwright, 1974; Deloya, 1994). The trophic diversity, for 12 h and preserved in 70% ethanol. The head capsule was worldwide distribution, relative abundance [e.g., Cart­ removed from the body and both parts were placed in warm po­ tassium hydroxide for a few minutes. Finally, they were rinsed wright (1974) collected about 275,000 specimens of with distilled water and placed in glacial acetic acid for two Ataenius simulator Harold in a light trap in a single night] minutes. Dissection took place under a binocular stereo­ and the high level of fecundity (Cambefort & Hanski, microscope (magnification up to 40 x), separate parts were stud­ 1991), could explain the potential of Ataenius species as a ied in temporary slides under a microscope using magnifications pest in areas recently transformed by man, such as the of 100 and 200 x. Drawings were made using FSA 25 PE tube golf course fairways, greens and tees in the United States (Leica). The light micrographs of thoracic spiracles and tegilla (Hoffman, 1935; Aim et al., 1992). It is very important to of the last abdominal segment were recorded on Ektachrome know both the larval stages of Ataenius and the biology 64T (Kodak) film with a photomicroscope Leitz DM-RB of the species in order to pursue studies of the dynamics (Leica) using interference contrast. Distinguishing characters that are readily seen using a binocu­ of their populations (Allsopp et ah, 1995). lar microscope (magnifications of 6 to 40 x) and subject to the In this study we describe the third larval instars of five least variation were mostly selected for use in the diagnosis of Ataenius species: Ataenius opatrinus Harold, A. picinus species. Extremely minute characters were used only if neces­ Harold, A. platensis (Blanchard), A. simulator Harold and sary. Most diagnostic characteristics are found on the head and A. strigicauda Bates. The larvae of the latter three species the mouthparts and on the ventral surface of the last abdominal were described by Jerath (1960), but the lack of illustra­ segment (Ritcher, 1966; Edmonds & Halffter, 1972, 1978; Kim tions makes identification very difficult. In this paper, we & Lumaret, 1988; Verdú & Galante, 1997). The morphology of give new descriptions and anatomical illustrations of the larvae was described using anatomical terminology of Jerath larvae studied. We also provide a key to the known larvae (1960), Ritcher (1966), Kim & Lumaret (1988) and Verdú & Galante (1997). According to Ritcher (1966), when the distance of Ataenius. between the two lobes of the respiratory plate of the thoracic MATERIAL AND METHODS spiracle ranges from 100 to 80% of the dorso-ventral diameter of the bulla, “equal to or slightly less than” has been used in de­ Breeding scribing the degree of constriction; “somewhat less than” is used Parental stock was collected in July, August and September when the distance is from less than 80 to 60%; “much less than” 1995 from Castillos, Minas, San Miguel de Salinas, and Colonia

57 0.25 mm

Figs 1-11: Ataenius opatrinus Harold. 1 - third instar larva, left lateral view; 2 - head, frontal view; 3 - antenna; 4 - right mandi­ ble, ventral view; 5 - right mandible, molar view; 6 - right mandible, dorsal view; 7 - left mandible, dorsal view; 8 - left mandible, molar view; 9 - left mandible, ventral view; 10 - left maxilla, dorsal view; 11- left maxilla, ventral view. Abbreviations: DES - dor- soepicranial setae; IVGS - interior ventral galea setae; LES - lateral external epicranial setae; ms - microsetae. when it is from less than 60 to 20%; and “almost contiguous” 2-4 microsetae on posterior part. Coronal suture present, when it is less than 20%. surpassing frontal suture. Clypeus transverse, on each RESULTS side one short anterior seta and one lateral seta. Labrum trilobed; on each side: one internal seta and on posterior Common morphological characteristicsof Ataenius part one long lateral seta; lateral lobe of the labrum with andAphodius larvae one seta; middle lobe of labrum with two anterior setae Body.Body arched (C-shaped) at the level of 4th or 5 th and one posterior seta. Antennae 4-segmented. Third seg­ abdominal segment (Fig. 1). ment with one ring of 5 setae and one well-developed Head. Cranium transverse, bearing on each side: one cone-shaped organ or one disc-like sensorial structure long seta on anterior frontal angle, a similar one on the (Verdu & Galante, 1997). Fourth segment short, with an lateral frontal part, one seta on anterior frontal region; a inner sensorial surface extended to dorsal and ventral posterior lateral seta on frontal region. Epicranial region: parts; apical end with one ring of sensorial setae, one minimum of two dorsoepicranial setae, 5-9 lateral setae, longer, whip-shaped. Mandibles: asymmetrical with two

58 14

0.25 mm 0.25 mm 15

Figs 12-17:Ataenius opatrinus Harold. 12 - epipharynx; 13 - hypopharynx; 14 - caudal view of last abdominal segment; 15 - raster; 16 - thoracic spiracle; 17 - palus. Abbreviations: ACP - acanthoparia; ACR - acroparia; BU - bulla; CLI - clithra; DAL - dorsal anal lobe; DX - dexiophoba; ETA - anterior epitorma; GL - glossa; LAL - lower anal lobe; LX - laeophoba; MIS - micro- sensillae; MPH - mesophoba; O - oncyli; PE - pedial area; PLA - palidium; PLG1S - posterior lateral glossae setae; PPH - proto- plioba; PTT - pternotormae; RSP - respiratory plate.

or three dorso-extemal setae and two microsensilla be­ by tegumental expansion. Glossa (GL) with two pairs of tween setae. Maxilla: galea and lacinia separated. Galea macrosensilla and a transversal row of microsensilla on with two dorsolateral setae and a variable number of in­ distal part of oncyli, proximal portion with a row of setae ternal setae; ventral portion with one longitudinal row of on each side; lateral lobe with 2 pairs of setae; central internal setae. Lacinia with trilobed uncus; a microseta at lobe with 4 setae and 4 macrosensilla. the base of each lobe; one row of setae situated dorsally, Thorax.Prothorax with a dorso-lateral plate lightly with short median seta on base; one basal seta on ventral sclerotized, straw-coloured. Concavities of respiratory portion; one basal seta on uncus. Stipes with a row of plates of thoracic spiracles facing posteriorly. Legs well- stridulatory teeth; one long lateral seta; two different developed; distal portions of tarsal claws generally sized fore setae and one small lateral microseta. Maxil­ curved, with two ventral setae. lary palpus 4-jointed; first joint (palpifer) with one ventral Abdomen. Concavities of respiratory plate of abdomi­ seta; third joint with two setae; fourth joint narrowed api- nal segments facing anteriorly. Raster with teges or with cally, with sensorial longitudinal area and distal ring of definite palidia. short microsetae. Epipharynx (Fig. 12) with anterior epi­ Distinguishing morphological characteristics of torma (ETA) situated in the central pedial area (PE), pter­ Ataenius and Aphodius larvae notormae (PTT) well-sclerotized. Mesophoba (MPH) with 3 pairs of macrosensilla covered by posterior expan­ To the naked eye, Aphodius and Ataenius larvae appear sions of tegument. Dexiophoba (DX) slightly more devel­ nearly identical. Nevertheless, several characteristics dif­ oped than laeophoba (LX). Protophoba (PPH) with ferentiate the two genera. expansions of integument and a transversal row of sen- Anal lobes.In Aphodius larvae, the lower anal lobe is silla. Haptomerum with one pair of macrosensilla. Ac­ cmarginate or entire; Ataenius larvae show two lower roparia (ACR) with 4 short setae. Chaetoparia (CPA) with anal lobes (LAL) (Fig. 14). The structure of the anal lobes small setae on each side. Acanthoparia (ACP) with one allows the diagnosis of larvae in vivo using only a bin­ short lateral seta. Clithra (CLI) well-developed. Hypopha­ ocular stereo-microscope (magnification 20 to 40 x). This rynx (Fig. 13): asymmetrical oncyli (O) covered in part characteristic has been previously used to identify closely related Aphodiinae species (Verdu et al., 1997).

59 0.25 mm Figs 18-28:Ataenius picinus Harold. 18 - third instar larva, left lateral view; 19 - head, frontal view; 20 - antenna; 21 - right mandible, ventral view; 22 - right mandible, molar view; 23 - right mandible, dorsal view; 24 - left mandible, dorsal view; 25 - left mandible, molar view; 26 - left mandible, ventral view; 27 - left maxilla, dorsal view; 28 - left maxilla, ventral view.

However, anal lobes are also good characteristics for the has been used (Ritcher, i 966; Verdu et al., !997). In definition of higher taxa (Ritcher, 1966). Aphodius and Ataenius we have found one constant dif­ Thoracic spiracles.The relative size and the number of ference in setation. In Aphodius, the interior dorsal galea “holes” of the spiracular respiratory plates are good char­ bears four setae while Ataenius has two setae (Fig. 10). acteristics for identifying closely related species of the Ataenius opatrinus Harold, 1867 same subgenus (Verdu et ah, 1997). Between the two Medium size (Fig. 1). Length of body 9.0-9.7 mm; genera, there are more differences related to the form of width of thorax 1.50-1.75 mm; maximum width of cra­ respiratory plates than the size or the number of holes on nium 1.42 mm. The larva of A. opatrinus presents the the plate. The respiratory plate in Aphodius is semicircu­ aforementioned common characteristics and the following lar, not surrounding the spiracular slit completely; diagnostic characteristics. whereas, in Ataenius, the respiratory plate is longer and Head. Epicranial region (Fig. 2) with 3-5 dorsoepicra- encircles the spiracular slit, in Ataenius species, there are nial setae (DES), 4-7 (6) lateral setae (LES) and 4 micro- usually fewer holes across the middle of the plate and setae (ms) on posterior part. Relation of lengths of the more holes across the arms of the plate. In Aphodius spe­ first, second and third segments of antenna is 1.4 : 1 ; 1 cies, there are more holes across the middle of the plate. (Fig. 3). Mandibles (Figs 4-9): Right mandible: Si and S2 Chaetotaxy.Within the Scarabaeidae, the setation of teeth fused; Si tooth isolated by one groove. Left rnandi- the venter of the last abdominal segment and of the head

60 32 34

0.05 mm

mm Figs 29-34: Ataenius piciims Harold. 29 - epipharynx; 30 hypopharynx; 31 - caudal view of last abdominal segment; 32 raster; 33 - thoracic spiracle; 34 - tegillum. ble: Si and S 2 teeth separated by a very small incision; S 3 mature instars occurred throughout the early spring. Lar­ tooth separated by shallow groove. Stipes of maxillae val development in laboratory lasted six weeks. Pupae with a row of 11-18 (13) stridulatory teeth (SD) (Fig. were observed in October. Ataenius opatrinus was col­ 10). Ventral portion of galea with one longitudinal row of lected from dry cattle dung at a forest edge. 7-8 internal setae (1VGS) (Fig. 11). Epipharynx (Fig. 12): Ataeniuspicinus Harold, 1867 Protophoba (PPH) with expansions of integument and Small size (Fig. 18). Length of body 8.5-9.2 mm; width 16-19 (17) sensilla. Hypopharynx (Fig. 13): Glossa with of thorax 1.5-1.7 mm; maximum width of cranium 1.30 14-16 (16) microsensilla on distal part of oncyli (MIS), proximal portion with 11-15 (12) setae on each side mm. (PLG1S). Head. Epicranial region (Fig. 19) with 4 dorsoepicra- Thorax. Diameter of the thoracic spiracle 0.10 mm; nial setae, 5-7 lateral setae and 2-3 microsetae on poste­ RSP (Fig. 16) with a maximum of 6-7 holes along any rior part. Relation of the lengths of the first, second and third segments of antennae is 1.6: 1 : 1.2 (Fig. 20). Man­ diameter. Distance of the two lobes of the respiratory plate much less than the dorsoventral diameter of the dibles (Figs 21-26): Right mandible: Si and S 2 teeth bulla. fused; S 3 tooth isolated by one groove. Left mandible: Si Abdomen. Lower anal lobe divided into two separated and S 2 teeth separated by small incision; S 3 tooth small and clearly separated by shallow groove. Stipes of maxil­ sublobes (Fig. 14). Raster (Fig. 15) with palidia (PLA) lae (Fig. 27) with a row of 18-22 (19) stridulatory teeth. nearly parallel, each palidium consisting of a rather Ventral portion of galea with one longitudinal row of 5 sparsely set row of 5 to 10 plume-like setae (Fig. 17). internal setae (Fig. 28). Epipharynx (Fig. 29): Protophoba Preseptular, hamate setae 36 to 47 in number (Fig. 15). with 17-19 sensilla. Hypopharynx (Fig. 30): Glossa with Material. 7 third instar larvae ex ovo, collected in Uruguay: 13-14 microsensilla on distal part of oncyli, proximal Lavalleja, Minas-Cerro Arequita, 2.ix. 1995, J.R. Verdu leg. portion with 7-8 (8) setae on each side. Voucher specimens are deposited in the entomological collec­ Thorax. Diameter of thoracic spiracle 0.08 mm; RSP tion of the Departamento de Ciencias Ambientales y Recursos Naturales, Universidad de Alicante (C.E.U.A.), Alicante, Spain. (Fig. 33) with a maximum row of 7 holes. Distance be­ Distribution. Ataenius opatrinus is known from Brazil, Ar­ tween the two lobes of the respiratory plate slightly less gentina (Blackwelder, 1944) and Uruguay. than the dorsoventral diameter of the bulla. Bionomics. Laboratory and field observations showed Abdomen. Lower anal lobe (Fig. 31) divided into two that the oviposition period was in September and the im­ separated sublobes. Venter of tenth abdominal segment

61 37

Figs 35—45: Ataenius platensis (Blanchard). 35 - third instar larva, left lateral view; 36 - head, frontal view; 37 - antenna; 38 - right mandible, ventral view; 39 - right mandible, molar view; 40 - right mandible, dorsal view; 41 - left mandible, dorsal view; 42 - left mandible, molar view; 43 - left mandible, ventral view; 44 - left maxilla, dorsal view; 45 - left maxilla, ventral view. without palidia (Fig. 32). Teges consisting of a patch of Ataenius platensis (Blanchard, 1846) short spatulate setae (Fig. 34). Small size (Fig. 35). Length of body 6.1-7.2 mm; width Material.3 third instar larvae ex ovo, collected in Uruguay: of thorax 1.0-1.3 mm; maximum width of cranium 1.15 Rocha, Castillos, 25.viii.1995, J.R. Verdu leg. Voucher speci­ mm. mens are deposited in the C.E.U.A. Head. Epicranial region (Fig. 36) with 4 dorsoepicra- Distribution.Ataenius picinus is known from Argentina, Bra­ zil, Uruguay (Blackwelder, 1944), the Antilles, New Zealand, nial setae, 5-6 lateral setae and 2-3 microsetae on poste­ Australia, Fiji Islands, New Caledonia (Chalumeau, 1983) and rior part. Relation of the lengths of the first, second and the USA (Cartwright, 1974). third segments of antenna is 1.5 : 1 : 1 (Fig. 37). Mandi­ bles (Figs 38-43): Right mandible: Si and S teeth fused; Bionomics. Oviposition occurred during September 2 S tooth isolated by one groove. Left mandible: Si and S and immature instars were found throughout early spring. 3 2 teeth separated by small incision; S tooth clearly sepa­ Larval development lasted approximately 5-6 weeks. Pu­ 3 rated by shallow groove. Stipes of maxillae with a row of pae were observed in October. Adults were collected 20-26 (23) stridulatory teeth (Fig. 44). Ventral portion of from dry cow dung, under carrion, associated with A. galea with one longitudinal row of 4-5 internal setae (Fig. platensis and the trogid Trox aeger Guérin. This species 45). Epipharynx (Fig. 46): Protophoba with 18-19 sen- is attracted to light, often in large numbers. silla. Hypopharynx (Fig. 47): Glossa with 12-15 micro-

62 48

0.25 mm

1 mm Figs 46-51:Ataenius platensis (Blanchard). 46 - epipharynx; 47 - hypopharynx; 48 - caudal view of last abdominal segment; 49 - raster; 50 - thoracic spiracle; 5 1 - tegillum. sensilla on distal part of oncyli, proximal portion with Ataenius simulator Harold, 1868 7-10 (9) setae on each side. Small size (Fig. 52). Length of body 5.8-9.0 mm; width Thorax.Diameter of thoracic spiracle 0.06 mm; RSP of thorax 1.1- 1.5 mm; maximum width of cranium 1.16 (Fig. 50) with a maximum row of 4-5 holes. Distance be­ mm. tween the two lobes of the respiratory plate somewhat Head. Epicranial region (Fig. 53) with 4 dorsoepicra- less than the dorsoventral diameter of the bulla. nial setae, 4-7 lateral setae and 2-3 microsetae on poste­ Abdomen. Lower anal lobe (Fig. 48) divided into two rior part. Relation of the lengths of the first, second and large separated sublobcs. Venter of the tenth abdominal third segments of antenna is 1.5 : 1 : 1.2 (Fig. 54). Mandi­ segment without palidia (Fig. 49); teges consisting of a bles (Figs 55-60): Right mandible: Si and S2 teeth fused; patch of 32-33 slender spatulate setae (Fig. 51). S 3 tooth isolated by one groove. Left mandible: Si and S: Material.5 third instar larvae ex ovo, collected in Uruguay: teeth separated by small incision; S 3 tooth clearly sepa­ Colonia de Sacramento, La Estanzuela, 29.ix.1995, J.R. Verdii rated by shallow groove. Stipes of maxillae with a row of leg. Voucher specimens are deposited in C.E.U.A. 10-23 (16) stridulatory teeth (Fig. 61). Ventral portion of Distribution. Ataenius platensis is known from Brazil, Ar­ galea with one longitudinal row of 5-6 internal setae (Fig. gentina, Uruguay (Blackwelder, 1944), Mexico, the Lesser An­ 62). Epipharynx (Fig. 63): Protophoba with 16-17 sen­ tilles (Deloya, 1994) and the USA (Cartwright, 1974). silla. Hypopharynx (Fig. 64): Glossa with 14-16 micro- Bionomics.Laboratory and field observations showed sensilla on distal part of oncyli, proximal portion with that the oviposition period was in September and imma­ 8-9 (8) setae on each side. ture instars occurred throughout early spring. Larval de­ Thorax.Diameter of thoracic spiracle 0.08 mm. RSP velopment in laboratory lasted six weeks. Pupae were (Fig. 67) with a maximum row of 5-6 holes. Distance be­ observed in November. Adults were collected from dry or tween the two lobes of the respiratory plate somewhat day-old cow dung in open pasture, under carrion, and at­ less than the dorsoventral diameter of the bulla. tracted to lights. Deloya (1994) captured this species with Abdomen. Lower anal lobe (Fig. 65) divided into two a necro-trap. big separated sublobes. Venter of tenth abdominal seg­ ment without palidia (Fig. 66). Teges consisting of a patch of 38-60 short spatulate setae (Fig. 68).

63 52

;C^mwn 0.25 mm

0.25 mm Figs 52-62:Ataenius simulator Harold. 52 - third instar larva, left lateral view; 53 - head, frontal view; 54 - antenna; 55 - right mandible, ventral view; 56 - right mandible, molar view; 57 - right mandible, dorsal view; 58 - left mandible, dorsal view; 59 - left mandible, molar view; 60 - left mandible, ventral view; 61 - left maxilla, dorsal view; 62 - left maxilla, ventral view.

Material.4 third instar larvae ex ovo, collected in Uruguay: Ataenius strigicauda Bates, 1887 Rocha, Castillos, 25.viii.1995, J.R. Verdu leg. Voucher speci­ Small size (Fig. 69). Length of body 7.0-8.7 mm; width mens are deposited in the C.E.U.A. of thorax 1.3-1.5 mm; maximum width of cranium 1.18 Distribution. Ataenius simulator occurs in Argentina (Black- welder, 1944), Mexico (Deloya, 1994), the USA (Cartwright, mm. 1974) and Uruguay, and has been introduced into Europe (Ba- Head. Epicranial region (Fig. 70) with 5 dorsoepicra- raud, 1992). nial setae, 5-8 lateral setae and 4 microsetae on posterior part. Relation of the lengths of the first, second and third Bionomics.Oviposition was in September; the imma­ segments of antenna is 1.6 : 1 : 1 (Fig. 71). Mandibles ture instars occurred throughout the early spring. Larval (Figs 72-77): Right mandible: Si and S2 teeth fused; S3 development lasted approximately 7 weeks. Pupae were tooth isolated by one groove. Left mandible: Si and S2 observed in October. Adults were collected from partly teeth separated by small incision; S3 tooth clearly sepa­ dry cow dung, but this species is rarely, if ever, a dung rated by shallow groove. Stipes of maxillae with a row of feeder; it is attracted to light, sometimes in enormous 19-28 (23) stridulatory teeth (Fig. 78). Ventral portion of numbers (Cartwright, 1974). galea with one longitudinal row of 4-5 internal setae (Fig. 79). Epipharynx (Fig. 80): Protophoba with 16-18 sen-

64 63 64 65

0.25 mm 0.25 mm

Figs 63-68:Ataenius simulator Harold. 63 - epipharynx; 64 - hypopharynx; 65 - caudal view of last abdominal segment; 66 - raster; 67 - thoracic spiracle; 68 - tegillum. silla. Hypopharynx (Fig. 81): Glossa with 14-15 micro- der decaying wood. This species was captured with a sensilla on distal part of oncyli, proximal portion with mosquito light trap (Deloya, 1994). 6-9 (8) setae on each side. Key to known third-instar/Dae/»«.? larvae (after Thorax. Diameter of thoracic spiracle 0.06 mm. RSP Jerath, 1960 and own results) (Fig. 84) with a maximum row of 6 holes. Distance be­ 1 Raster with palidia ...... A. opatrinus Harold tween the two lobes of the respiratory plate slightly less — Raster without palidia ...... 2 than the dorsoventral diameter of the bulla. 2 Epicranial region with 3 dorsoepicranial setae ...... 3 Abdomen. Lower anal lobe (Fig. 82) divided into two — Epicranial region with more than 3 dorsoepicranial setae 6 large separated sublobcs. Venter of tenth abdominal seg­ 3 Raster with teges of 28-35 setae; blunt stridulatory teeth on ment without palidia (Fig. 83); teges consisting of a patch stipes 8-10 ...... A. saxatilis Cartwright of 34-45 fairly short spatulate setae (Fig. 85). — Raster with teges of more than 34 setae; stipes with more than 10 stridulatory teeth ...... 4 Material.4 third Instar larvae ex ovo, collected in Uruguay: 4 Maxillary stridulatory area with an irregular row of 13-19 Rocha, Los Ajos, S.vlii. 1995, J.R. Verdu leg. Voucher speci­ conical teeth ...... A. ovatulus Horn mens are deposited in the C.E.U.A. — Stridulatory teeth on stipes 20 or more ...... 5 Distribution. Ataenius strigicauda is known from Mexico, 5 Raster with teges of 44-50 hamate setae. Width of head cap­ Guatemala, Honduras, Nicaragua, Panama, Trinidad, Brazil, Bo­ sule 1.32-1.35 mm. Maxillary stridulatory area with an ir­ livia, Argentina, the Bahama islands, Cuba, Jamaica, regular row of 24-28 conical teeth ...... A. erratus Fall Hispaniola, Puerto Rico, St. Thomas (West Indies), St. Croix — Raster with teges of 34-43 hamate setae. Width of head cap­ (Virgin Islands), Guadeloupe, Dominica, St. Lucia, Barbados, sule 1.02-1.12 mm. Stridulatory teeth on stipes 21-24 .... St. Vincent, Bequia (Grenadines), Grenada (Blackwelder, ...... A. imbricatus (Melsheimer) 1944), the USA (Jerath, I960) and Uruguay. 6 Epicranial region with 4 dorsoepicranial se ta e ...... 7 Bionomics. The oviposition period was in September; — Epicranial region with 5 dorsoepicranial setae ...... 9 the immature instars occurred throughout the early spring. 7 Distance between the two lobes of the respiratory plate Larval development lasted approximately four weeks. Pu­ slightly to much less than the dorsoventral diameter of the pae were observed in October. Adults were collected un­ bulla. Respiratory plate with maximum row of 7 holes ...... A. picinus Harold

65 0.25 mm Figs 69-79:Ataenius strigicauda Bates. 69 - third instar larva, left lateral view; 70 - head, frontal view; 71- antenna; 72 - right mandible, ventral view; 73 - right mandible, molar view; 74 - right mandible, dorsal view; 75 - left mandible, dorsal view; 76 - left mandible, molar view; 77 - left mandible, ventral view; 78 - left maxilla, dorsal view; 79 - left maxilla, ventral view.

— Distance between the two lobes of the respiratory plate sidered this species as belonging to the genus Parataenius equal to or slightly less than the dorsoventral diameter of the Balthasar (Dellacasa, 1987), while others included it bulla. Respiratory plate with maximum row of 4-6 holes . 8 among Ataenius species (Cartwright, 1974; Deloya, 8 Raster with teges of 32-33 setae; stipes with 20-26 blunt 1994). Our results showed few differences between the stridulatory teeth ...... A. platensis (Blanchard) larvae o f Ataenius studied and A. simulator. Only A. — Raster with teges of 38-60 setae; stipes with 10-23 blunt stridulatory teeth ...... A. simulator Harold opatrinus showed some peculiar traits, such as the pres­ 9 Stipes with 9-11 blunt stridulatory teeth .... /I. brevis Fall ence of palidia and the shape of respiratory plate, but — Stipes with 19-28 stridulatory teeth .. A. strigicauda Bates these characteristics often distinguish the larvae of closely related species (Ritcher, 1966; Verdu et al., 1997). Ac­ DISCUSSION cording to our results, A. simulator and A. opatrinus Morphological relationships should be classified in Ataenius. Keys are generally considered artificial and not in­ The morphology of the studied Ataenius larvae is more tended to show phylogenetic relationships, but this is fre­ homogeneous than is seen in the Aphodius larvae (Madle, 1935, 1936; Jerath, 1960; Ritcher, 1966; Walter, 1982; quently apparent. Our results did not show phylogenetic relationships among the Ataenius species. Nevertheless, Kim & Lumaret, 1986; Verdu & Galante, 1995, 1997). our data allowed us to reconsider the inclusion of A. This is probably a consequence of their feeding patterns. simulator within the genus Ataenius. Some authors con­ Many species, particularly the species of Apho­ dius, show coprophagous habits, which is a derived feed-

66 Figs 80-85:Ataenius strigicauda Bates. 80 - epipharynx; 81 - hypopharynx; 82 - caudal view of last abdominal segment; 83 - raster; 84 - thoracic spiracle; 85 - tegillum. ing behaviour from the primitive saprophagous habits of REFERENCES the Aphodiinae (Halffter & Edmonds, 1982). However, Allsopp P.G., N iemczyk H.D. & K lein M.G. 1995: Sampling the , especially the species of Ataenius, are basi­ distributions and sequential sampling for third instars of black cally saprophagous (Cambefort, 1991), feeding efficiently turfgrass Ataenius, (Haldeman), in control on humus. Their larvae also occasionally eat roots (Weg­ trials. Pedobiologia 39: 126-131. ner & Niemczyk, 1981; Cambefort, 1991; Ratcliffe, Ai.m S.R., Y eii T., Hanula J.L. & G eorges R. 1992: Biological 1991). The evolution from saprophagy to coprophagy was control of Japanese, oriental, and black turfgrass Ataenius the most important shift involving the species diversifica­ (Coleóptera: Scarabaeidae) larvae with entomopatho- tion of laparostict (Cambefort, 1991; genic nematodes (Nematoda: Steinernematidae, Heterorhabdi- tidae). J. Econ. Enlomo!. 85: 1660-1665. Scholtz & Chown, 1995). This evolutionary trend re­ Baraud J. 1992: Coléoptères Scarabaeoidea d’Europe. Faune de quired ethological, physiological and morphological di­ France 78. France et régions limitrophes. Fédération versification with special modification of the mouthparts Française des Sociétés de Sciences Naturelles, Paris, et Soci­ (Halffter & Matthews, 1966; I lata & Edmonds, 1983; été Linnéenne de Lyon, Lyon, 856 pp. + 11 pis. Stebnicka, 1985), while the saprophagous species re­ B eackwuldhr R.E. 1944: Checklist of the coleopterous tained more primitive and undifferentiated mouthparts. of Mexico, Central America, the West Indies and South America. U. S. Natl. Mus. Bull. 185: 197-265. ACKNOWLEDGEMENTS. We are indebted to E. Morelli Cambefort Y. 1991 : From saprophagy to coprophagy. In Hanski (Universidad de la República Oriental del Uruguay) for his help I. & Cambefort Y. (eds): Ecology. Princeton and hospitality during the visit of JRV to Uruguay in 1995. We University Press, Princeton, New Jersey, pp. 22-35. also thank Z. Stebnicka (Institute of Systcmatics and Evolution C ambefort Y. & Hanski I. 1991: Dung beetle population biol­ of , Polish Academy of Sciences) for confirmation of ogy. In Hanski 1. & Cambefort Y. (eds): Dung Beetle the identification of Ataenius species. K. Burke checked the Ecology. Princeton University Press, Princeton, New Jersey, English version of the manuscript. The stay of JRV in Uruguay pp. 36-50. was funded by an “lntercampus/E.AL.’95” grant from the AECI C arne P.B. 1951: Preservation techniques for scarabeid and (Spanish Ministry of Foreign Affairs). other larvae. Proc. Linn. Soc. N. S. W.76: 26-30.

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